Gall midges belong to the family Cecidomyiidae within the order Diptera. A gall midge life cycle consists of four separate stages: egg, larva, pupa and adult. The adult stage normally lasts only for a few days and during this period most gall midges do not feed. Adults are small, delicate flies measuring only a few millimeters in length. Gall midges exist all over the world and approximately 4,500 species are known, but probably many more exist. The Cecidomyiidae is a highly diverse family, including species that feed on plants, animals and fungi. Many of the plant-feeding gall midges are considered major agricultural pests.
The Hessian fly, Mayetiola destructor (Say) is one of the most destructive pests on wheat (Triticum spp) in the United States and North Africa, but it is also considered a pest in many European countries. Wheat is the most widely cultivated crop in the world, providing 20 percent of the calories consumed, and the Hessian fly is present in most of the major wheat growing areas. It is believed that the fly originated in Southwest Asia where wheat also originated. Since then, it has spread and its distribution today is almost global, ranging from North America in the west, throughout Europe and all the way to Siberia in the east. It can also be found as far south as Morocco, Cyprus and Iraq. On the southern hemisphere it is found on New Zealand. In North America it was probably introduced by Hessian soldiers during the war of Revolution or Independence in the 1700s. Therefore, the name Hessian fly was given to it 1778, although the first scientific description was not provided until 1817 by Thomas Say.
Although wheat is the preferred host, other grasses in the tribe Triticeae such as rye (Secale cerale L), barley (Hordeum vulgare L) and wild grasses, can also be used as hosts. Rye is the second most preferred host. In contrast, oat (Avena sativa L, tribe Aveneae) does not support development of Hessian fly larvae.
Life Cycle
Adult female Hessian flies emerge with a full complement of mature eggs Within a few minutes after emergence, females position themselves in a calling posture with their ovipositors extended and release a sexual pheromone to attract males When males sense the pheromone, they fly upwind towards the female Once a female is located, mating occurs quickly No male courtship behaviour occurs and females are almost always receptive on the first contact with a male Males mate several times if opportunity is given In contrast, females mate only once When mating is initiated, the female retracts her ovipositor and after mating, she sits inactive with her ovipositor retracted until oviposition begins 1 5-5 hrs later If females are not mated on their first day, they stop calling at about 113O h On day two they resume calling at about 0100 h and stop at about 1200 h with a peak between 0600-0800 h In virgins, this cyclic calling pattern is repeated at day three and four and continues until death, although virgins may start to lay unfertilized eggs at day three or four Mated females carry 50-400 eggs and oviposit on wheat leaves or some other possible host Normally, individual females produce unisexual progenies (all-male or all-female) The sex that is produced depends on the maternal genotype and is dependent on maintenance or elimination of the paternally derived sex chromosomes, which result in female and male progeny, respectively However, sometimes both sexes are produced, but then one sex often predominates Hessian fly eggs hatch after 3-5 days (FIG. 1) Soon after hatching on a leaf, the first instar larva migrates down the plant between the leaf sheets until it reaches the base of the plant where it establishes a feeding site, starts to feed and moults This is the only movement the larva does and it is thus restricted to the plant its mother chooses The second instar continues to feed and grow until it enters the third stage The duration of the larval feeding period ranges from 9-17 days The third non-feeding, immobile stage develops inside the second instar's skin, which is retained and scierotized to form a pupaπum, the so called “flaxseed” The pupa then develops, still inside the skin of the second larval instar The flaxseed stage normally lasts for about 12 days, but this varies depending on environmental conditions The adults emerge from the flaxseeds to complete the life cycle Adult males live for 1-2 days and virgin females for 3-4 days Mated females do not live as long as virgins and generally have less than a day to lay their eggs after mating One lifecycle can be completed in 20 days when conditions are optimal, but may also take up to 42 months if the third larval instar diapauses Generally, all stages develop faster in warm and moist conditions, whereas dry and cool as well as dry and hot weather will increase the generation time
The number of generations per year ranges from one to six During the flaxseed stage, prevailing climatic conditions (i e temperature and relative humidity) determine if the larvae
go through direct development, aestivation (oversummering) or diapause (overwintering). Since the climate determines the extent of aestivation and diapause, the number of generations per year is also dependent on the local climate. The number of generations and patterns of aestivation and diapause vary with latitude throughout North America.Hessian Fly Damage and Deployed Control Methods
Damage from Hessian fly infestations can be quite extensive. When the larva has reached its feeding site it secretes a salivary substance that elicits release of plant nutrients. An attack results in differentiation of nutritive tissue around the feeding site and the larva is provided with a diet rich in amino acids and sugars. Hessian fly larval feeding does not result in macroscopic gall formations, instead the galls produced are referred to as simple galls. Plant cells below the attacking larva are inhibited from further growth, but are kept alive and are under constant stress from the larva. Larval feeding results in stunted growth. The stalks become weak and may break and if a seedling is attacked it normally dies. Moreover, attack on older plants result in fewer and/or smaller seeds, or seeds of low quality. Hessian fly infestations normally result in yield losses of economic importance, especially when infestation levels are high. In Morocco, an estimate of 32% of the wheat yield have been lost due to fly infestations and the outbreak 1988-1989 caused a $20 million loss in Georgia, USA. Clearly, Hessian fly populations must be controlled, but no control method used today is efficient enough.
Two main control methods are commonly used in the USA: (i) delayed planting and (ii) resistant wheat varieties. To some extent insecticides are used as well. These methods all have some disadvantages. The usage of delayed planting or “fly-free” planting dates to avoid fall infestations have been used since 1799. Hessian flies emerge during fall from old wheat stubble, volunteer wheat or from other grass hosts. By planting after fly activity has ceased, female flies are forced to lay their eggs on other hosts than wheat. This method has successfully reduced fall infestations in the northern USA where only one fall generation occurs and the fly diapauses during winter. However, by delaying planting in the southern parts of USA where additional fall and winter generations exist, fall damage is normally reduced, but the risk of spring damage is increased. Moreover, recommended planting dates are based on typical years and may not be effective if emergence is late. An additional problem with this method is that the later planting date reduces yield since the growth season is shortened and the risk of cold injury increases.
While delayed planting is of limited use and normally only affects fall infestations, using wheat cultivars resistant to Hessian fly attack provide full season control and has been the most effective and economic control method So far, 29 different resistance (R) genes have been found By incorporating one of these into the cultivated wheat variety, Hessian fly larvae do not establish or grow and typically die within two to five days after arrival at the feeding site The problem is that the R genes impose a heavy selection pressure on the flies that evolve to become more virulent and eventually overcome the resistance In Indiana 1955, a cultivar carrying an R gene was deployed and provided efficient resistance However, after six years the flies had evolved counter-resistance Then a cultivar carrying a second R gene was released 1964, with counter-resistance appearing within eight years 1971, a third gene was released and counter-resistance had evolved within 10 years Due to the deployment of different resistant wheat cultivars, 16 Hessian fly biotypes in the USA have evolved that only differ in their ability to infest and survive on specific resistant wheat varieties As a consequence, new R genes must constantly be identified and incorporated into wheat cultivars This is very costly and time consuming, and it is often difficult to combine resistance with satisfactory straw strength, earliness and grain quality As a result, resistant wheat normally gives lower yield compared to susceptible cultivars when Hessian fly damage is absent Moreover, R genes are thought to be of limited numbers and should not be wasted
Although not widely practiced, spraying insecticides at planting have the potential to reduce fall, winter and spring damage without subsequent yield losses But, since early infestations of Hessian fly are extremely difficult to detect, insecticides must be used as a preventative strategy Besides the potential negative effects on the environment and farmers' health, spraying insecticides also kills the flies' parasitoid enemies In addition, insecticide usage when it is not needed is an unnecessary cost for the farmer.
Sexual Pheromones in Hessian Fly Control
Early infestations of Hessian fly are difficult to detect for several reasons First, all life stages are very small, adults have a highly synchronized eclosion and flight activity, and may be present in the crop for a very short period of time due to their short lifespan Second, the larvae feed inside the stem, the damage they produce is subtle and the young plants often give a false impression of well-being due to their erectness and darkish-green colouration As a consequence, flies are normally detected after they have become a serious problem Third, outbreaks are typically sporadic and hence difficult to predict The aestivation and diapause habits of the fly make them survive unfavourable environmental conditions for long periods When conditions return to favourable, aestivation or diapause is terminated, and suddenly flies are present in the crop again
Female sex pheromones for control of Hessian fly populations are a realistic solution to the control problems, without direct negative effects on the environment. By using traps baited with synthetic versions of the pheromone, useful information about the Hessian fly population can be obtained. The traps can be used to detect the presence of flies as well as the timing of their flight activity in the field. Moreover, traps can be used to estimate population levels to decide if other control methods (e.g. resistant wheat varieties or insecticides) are necessary and/or economical. If a pheromone based monitoring system was used, the farmer would have the ability to avoid unnecessary yield losses and environmental pollution. However, the sex pheromone must be chemically identified before it can be used in a monitoring system. Once the pheromone is identified, pheromone based monitoring is a method that can be used by the individual farmer. It does not require entomological skills since the pheromone is species specific. In addition, pheromones can be used in an attract-and-annihilate method, where males are attracted to a site where they are removed from the environment (i.e. killed). Mating disruption is another method that can be used for control of pest populations. In this method, synthetic pheromones are released at a high enough amount to disrupt mate finding. It is however unclear if the attract-and-annihilate method and mating disruption can be used for Hessian fly control. Both methods are used to reduce pest populations and they are most efficient at low population densities. Therefore, they have greater utility in preventing outbreaks (which may not be economical for Hessian fly control), rather than reducing the population during an outbreak. An additional problem with the use of these methods for Hessian fly control is the practice of crop rotation. The attract-and-annihilate method or mating disruption must be carried out in the emergence field, and if crops are rotated, flies might not emerge in a wheat field. Therefore, the deployment of these methods might be difficult, especially if the farmers are unwilling to control an insect that is pest of a crop that they are not currently growing.
Pheromone based monitoring systems have been developed and commercialized for at least two Cecidomyiids: the pea midge, Contaηnia pisi (Hillbur et al 2000) and the swede midge C. nasturtii (Hillbur et al 2005), although opportunities exist for the orange wheat blossom midge, Sitodiplosis mosellana, Douglas-fir cone gall midge, C. oregonensis, red cedar cone midge, Mayetiola thujae, and the aphidophagous gall midge, Aphidoletes aphidimyza. 
The Hessian fly pheromone To date, 13 cecidomyiid species are known to use sex pheromones, however, pheromone compounds have been identified only for seven of those (Table 1). The identified cecidomyiid pheromone compounds show a striking similarity in their chemical structure.
Most compounds are 13-carbon chains with a functional group (often an acetate group) in C-2 position, although some species have shorter or longer carbon chains.
TABLE 1Species in Cecidomyiidae known to have sexualpheromones (modified from Hillbur 2001).CompoundLaboratoryidentifi-SpeciesField trappingbioassayscationHessian flyCartwright (1922)McKay and Foster et al Mayetiola destructorHatchett (1984)(1991b)Harris and Foster (1991)Red cedar coneGries et al (2005)Gries et al midge(2005)Mayetiola thujaeBrassica pod midgeWilliams (1990)Williams and Dasineura brassicaeMartin (1986)Blackcurrant leafGarthwaite andmidgeWall (1986)Dasineura tetensiApple leaf curlingHarris et al (1996)Harris et al midge(1996)Dasineura maliDouglas-fir cone gallMiller and BordenMiller and Gries et al midge(1981)Borden (1984)(2002)ContariniaGries et al (2002)oregonensisPea midgeWall et al (1985)Hillbur and Hillbur et al Contarinia pisiHillbur et al (2000)Löfqvist (1996)(1999)Hillbur et al (2000)Sorghum midgeSharma andContarinia sorghicolaVidyasagar (1992)Swede midgeHillbur et al (2005)Hillbur et al Hillbur et al Contarinia nasturtii(2005)(2005)Orange wheatPivnick (1993)Pivnick Gries et al blossom midgeGries et al (2000)(1993)(2000)Sitodiplosis mosellanaPine gall midgeLee and Lee Thecodiplosis(1985)japonensisRice midgeSain and KalodeOrseolia oryzae(1985)Aphidophagous gallChoi et al (2004)Choi et al Choi et al midge(2004)(2004)Aphidoletesaphidimyza
The first observation that indicated that Hessian fly females release a long-range sex pheromone was done by Cartwright (1922) He placed cages containing females in the field and observed that males flew upwind towards the females at distances within 15 feet Decades later it was shown, in a Y-tube olfactometer bioassay, that males were attracted to females with extended ovipositors as well as to hexane washes of female ovipositors. They also found that female sexual attractiveness and mating activity seemed to be regulated by extension and retraction of the ovipositor and that female attractiveness followed a diurnal rhythm. Their results suggested that the ovipositor is the pheromone release site. Later it was found that the ovipositor contains gland tissue, indicating that it is also the site of pheromone production.
The first compound in the Hessian fly pheromone to be identified was (2S,10£)-10-tridecen-2-yl acetate (2S-E10-13:OAc). Virgin females were shown to contain a relatively large amount (ca 2 ng) of this compound shortly after emergence and then declining amounts for at least the next 8 hours of the photophase. However, in the early mornings of the second and third days, the amount of pheromone in virgins was high again and with the same patterns of declining amounts during subsequent hours. In contrast, mated females do not continue to produce pheromone.
The attractiveness of 2S-E10-13:OAc to male Hessian flies was studied in a wind tunnel by Harris and Foster (1991). Only 56% of the males contacted the odour source when 2S-E10-13:OAc was used as stimulus, whereas 87% contacted the source when female ovipositor extract was used. This result indicated that the sex pheromone consists of at least one additional compound. Thus the male response was also measured to binary blends of 2S-E10-13:OAc and racemic mixtures of three other chemicals, found in female extract: (10Z)-10-tridecen-2-yl acetate (Z10-13OAc)1 (10E)-10-tridecen-2-ol (E10-13OH) and tridecan-2-yl acetate (13:OAc).
However, none of these blends attracted more males than did 2S-E10-13:OAc alone. In a field study, the main compound (2S-E10-13:OAc) did not catch any male Hessian flies, but instead caught another so far unidentified cecidomyiid. Additional results from a semi-field test (Hillbur et al unpublished) have shown that a tertiary blend of 2S-E10-13:OAc, 2S-E10-13OH and 2S-13:OAc caught significantly more males than the main compound alone and blank traps. Furthermore, coupled gas chromatographic-electroantennographic detection (GC-EAD1 Arm et al 1975) has shown that these three compounds elicit antennal responses in male Hessian flies (Hillbur et al unpublished).
However, the three-component blend has not been tested behaviourally under controlled laboratory conditions and its attractiveness has not been compared to female pheromone extract. GC-EAD analyses of female extract have also revealed additional, so far unidentified compounds that elicit antennal responses. Chemical analyses of gland extract have shown that one of the unidentified compounds is a double-unsaturated C13 acetate. An unsaturated C15 acetate has also been found in gland extract, but it is not known if it corresponds to one of the antennally active compounds. The chemical identification of these compounds is difficult since they exist in minute amounts in female extract. Because of this, the stereochemistry and the position of the double bonds are unclear, but four candidate compounds have been proposed (Hillbur et al unpublished).